Wolbachiainfection reduces sperm competitive ability in an insect

Abstract

The maternally inherited bacterium Wolbachia pipientis imposes significant fitness costs on its hosts. One such cost is decreased sperm production resulting in reduced fertility of male Drosophila simulans infected with cytoplasmic incompatibility (CI) inducing Wolbachia. We tested the hypothesis that Wolbachia infection affects sperm competitive ability and found that Wolbachia infection is indeed associated with reduced success in sperm competition in non-virgin males. In the second male role, infected males sired 71% of the offspring whereas uninfected males sired 82% of offspring. This is the first empirical evidence indicating that Wolbachia infection deleteriously affects sperm competition and raises the possibility that polyandrous females can utilize differential sperm competitive ability to bias the paternity of broods and avoid the selfish manipulations of Wolbachia. This suggests a relationship between Wolbachia infection and host reproductive strategies. These findings also have important consequences for Wolbachia population dynamics because the transmission advantage of Wolbachia is likely to be undermined by sperm competition.

The dynamic relationship between polyandry and selfish genetic elements

“…Uninfected females do not discriminate against infected males as mates [54]. However, infected males are poor sperm competitors relative to uninfected males [39]. Uninfected females mating multiply with at least one uninfected male are able to recuperate their fitness loss caused by CI owing to the poor sperm performance of infected males, and have the same reproductive output as infected females (figure 1a,b).…”

“…Although there are benefits of Wolbachia infection in terms of conferring protection against RNA viruses in both fly species [84,85], this benefit is enjoyed by both sexes and cannot explain why infected males should mate at a higher rate than uninfected males (and endosymbiont protection against viruses is not universal [86]). In addition, infected D. simulans males suffer reduced sperm production [61] and sperm competitive ability [39] relative to uninfected males, further suggesting that Wolbachia infection is not associated with a reproductive advantage to males. This result taken together with the finding that uninfected D. simulans females remate sooner (the only ones at risk of CI), suggests that Wolbachia infection can favour both male and female multiple mating as a strategy to avoid associated reproductive incompatibilities, but that the impact differs depending on the infection status.…”

Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

“…Aside from reproductive manipulations, Wolbachia has also been linked with reduction of sperm production (Snook et al, 2000) and sperm competitive ability (de Crespigny and Wedell, 2006) in D. simulans males. In CI-inducing Wolbachia, lower sperm competitiveness may undermine the effects of the reproductive manipulations and alter Wolbachia spread dynamics.…”

Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue

“…Recent studies demonstrate that Wolbachia influences olfactory-cued locomotion (Peng et al, 2008) and mating behavior (Champion de Crespigny and Wedell, 2006;Gazla and Carracedo, 2009;Koukou et al, 2006). It is well known that distinct elements of the Drosophila brain govern certain behavior, especially well characterized are sex-specific behaviors such as courtship (Hall, 1979;Villella and Hall, 2008).…”